Many authors (Hering, 1927; Koch 1931; Heymans, Bouckaert & Regniers,
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1 259 J. Physiol. (I949) I09, I 6I2.0I :6I2.I4 PRESSOR RESPONSES TO ELECTRICAL STIMULATION OF THE CAROTID SINUS NERVE IN CATS BY E. NEIL AND C. R. M. REDWOOD Department of Physiology, School of Medicine Leeds AND A. SCHWEITZER Department of Physiology, University College, London (Received 26 February 1948) Many authors (Hering, 1927; Koch 1931; Heymans, Bouckaert & Regniers, 1933; Schweitzer, 1937) describe the response of the carotid sinus nerve receptors to change of pressure in the isolated carotid sinus, and show clearly that these nerve endings act as baroceptors so that a rise of intrasinusal pressure causes, reflexly, a fall of systemic blood pressure. Action potential studies by Bronk & Stella (1932) support this view: a rise of pressure in the sinus is attended by an increased frequency of impulses in the afferent fibres of the carotid sinus nerve. It is generally agreed that the baroceptors are stimulated only by a rise of pressure in the sinus, and evidence exists that there is a threshold pressure (20-80 mm.hg in different species) below which activation of the baroceptors does not occur (Koch, 1931; Schweitzer, 1937). In view of the large number of observations on carotid sinus function, it is perhaps surprising that there are only few observations with reference to the effects of electrical stimulation of the nerve trunk. The development of the rectangular wave electronic stimulator permits a more detailed investigation of this problem, and the present paper gives results obtained by the use of this device and of a conventional induction coil. Some of our observations have previously been reported (Neil, Redwood & Schweitzer, 1948). METHODS Forty-five cats were used in these experiments. The animals were anaesthetized with chloralose (0*08-0*1 g./kg. body weight, intravenously), chloral hydrate (0-15-0*2 g./kg. body weight, intravenously) or nembutal (Pentobarbitone sodium) (35-40 mg./kg. body weight, intraperitoneally). In other experiments cats were decerebrated under light ether anaesthesia; at least 60 min. were allowed for the effects of the volatile anaesthetic to pass off before experimentation was started. In a number of decerebrate cats either chloralose or nembutal was injected at a later stage of the experiments. PH. CIX. 17
2 260 E. NEIL, C. R. M. REDWOOD AND A. SCHWEITZER The carotid sinus nerve was prepared for stimulation using an approach similar to that described by Von Euler, Liljestrand & Zotterman (1939). The glossopharyngeal nerve was dissected free and the carotid sinus nerve carefully bared from its junction with the glossopharyngeal nerve down to the tissue lying in the region of the common carotid artery bifurcation. Fine shielded silver wire electrodes mounted in perspex were used for stimulation of the carotid sinus nerve. In most experiments a rectangular wave electronic stimulator which allowed independent variations of frequency of stimulation ( cyc./sec.), pulse duration ( msec.) and voltage output (1-100 V.), was used. In some experiments an ordinary induction coil was used. The carotid sinus nerve was stimulated for periods of sec. In other experiments, the carotid sinus was isolated from the general circulation by ligaturing all branches of the common carotid artery and finally tying off the common carotid itself. A glass cannula was introduced into the common carotid artery and connected to a pressure bottle containing oxygenated buffered Ringer-Locke solution, which allowed rapid changes in pressure to be effected (Moissejeff, 1926; Koch, 1931; Schweitzer, 1937). The pressure in the sinus was recorded from a manometer connected to a side-arm of the cannula. An alternative method consisted in the perfusion of the isolated carotid sinus by gravity flow. The perfusion fluid left the sinus through a cannula inserted into the external carotid artery. The outflow tube was fitted with a screw clip which allowed variable resistance to flow. The perfusion pressure was recorded from a manometer attached to a side-arm of the outflow cannula. Blood pressure was recorded from a femoral artery. Heart-rate changes were observed from blood-pressure records obtained with fast kymograph speeds. As an anticoagulant a continuous intravenous drip of heparin was given in many experiments. A tracheal cannula was inserted. Respiration was recorded by stethograph or closed circuit Krogh spirometer filled with 02, CO. being absorbed by soda lime. RESULTS Electrical stimulation of the carotid sinus nerve Chloralose anaesthesia. In all but two of the experiments, stimulation of the carotid sinus nerve in cats under chloralose anaesthesia, using the rectangular wave stimulator (100 cyc./sec., msec. pulse duration, 1-3 V.) or an induction coil discharge, produced a marked rise in arterial blood pressure (Fig. 1). This rise was rapid and its extent was found to be dependent mainly upon the pulse duration of the stimulus emploved. Maximal responses ( mm. Hg) were usually obtained with stimuli of msec. duration. It was found that the extent of the blood-pressure rise following stimulation of the carotid sinus nerve was independent of the initial blood-pressure level. The rise of arterial blood pressure thus produced was fairly well sustained during a 30 sec. period of stimulation. On discontinuing the stimulation the blood pressure rapidly fell to its orginal level. Pressor responses were also obtained with the use of the induction coil stimulator. In the experiments with the rectangular wave stimulator, the pressor response appeared to be independent of the frequency of stimuli above a threshold value of approximately 50 cyc./sec. Similarly, voltage outputs greater than 1 V. did not appreciably alter the characteristics of the response.
3 STIMULATION OF THE CAROTID SINUS NERVE 261 This phenomenon was independent of respiratory variations concomitantly produced by sinus-nerve stimulation. The rate and amplitude of respiration, Fig. 1. Cat, chloralose. Records from above downwards: blood pressure, signal, time in 5 sec. Rectangular wave stimulation of right carotid sinus nerve with 100 cyc./sec., 2V., and pulse durations of 0-05, 0.5, 1-0 and 0.1 msec. Fig. 2. Cat, chloralose. Records from above downwards: respiration (Krogh spirometer), blood pressure, time in 5 sec., signal. Stimulation of right sinus nerve with induction coil discharge (coil distance 12 cm.) A, slow speeds; B, fast speeds. Note absence of conspicuous cardiac slowing or respiratory disturbance. though commonly increased, varied considerably in different animals. The pressor response to carotid sinus-nerve stimulation, however, was equally well obtained when little or no hyperpnoea was observed (e.g. Fig. 2). 17-2
4 262 E. NEIL, C. R. M. REDWOOD AND A. SCHWEITZER The pressor response was unaffected by double vagotomy, destruction of the contralateral carotid sinus nerve, section of the homolateral glossopharyngeal nerve peripheral to its junction with the carotid sirdus nerve, homolateral cervical sympathectomy, sectioning of the homolateral carotid sinus nerve near its origin from the carotid sinus, and bilateral. adrenalectomy. The, pressor response to carotid sinus-nerve stimulation was abolished by high cervical spinal transection or section of the glossopharyngeal nerve central to its junction with the carotid sinus nerve. Fig. 3. Cat, chloralose. Records from above downwards: respiration, blood pressure, signal, time in 5 sec. Rectangular wave stimulation of right carotid sinus nerve (100 cyc./sec., 2V., and pulse durations of 0-05, 1.0, 0.5 and 0 1 msec.' Note pressor responses to short, depressor responses to long pulses. Marked response to occlusion of right common carotid artery (signal 5). Noteworthy changes in heart rate were not observed in experiments where carotid sinus nerve stimulation produced a marked rise in arterial blood pressure (Fig. 2). The response to carotid sinus-nerve stimulation using the rectangular wave stimulator was found to depend on the pulse duration. Fig. 3 shows the effect of varying the pulse duration of the stimulus, frequency and voltage of stimuli remaining constant (100 cyc./sec., 2 V.). In this experiment pulse durations of msec. produced the usual rise, longer pulses ( msec.) a fall in arterial blood pressure. In other animals, use of the longer pulse durations ( msec.), though not producing a fall of blood pressure, failed to cause
5 STIMULATION OF THE CAROTID SINUS NERVE 263 such a pronounced rise of pressure as was obtained with stimuli of 0.1 msec. duration., These unexpected results led to an investigation as to the effect of the anaesthetic used. Decerebrate cats. The experiments were repeated in decerebrate cats, stimulation of the carotid sinus nerve intermittently being carried out over a period of several hours. Invariably, such stimulation caused a marked fall in arterial blood pressure, attended by cardiac slowing. This fall in blood pressure was independent of the frequency or pulse duration of the stimuli used. However, ~~~~~~~~~~~~~~~~~~ as Fig. 4. Decerebrate cat. Records from above dow-nwards: blood pressure, time in 5 sec., signal. Tracing A: induction coil stimulation of right carotid sinus nerve (coil distance 15 cm.). Tracing B: repeat stimulation 30 min. after intravenous injection of chiloralose (0.1 g./kg. body wt.) the intravenous injection of > 0'05 g. of chloralose into these decerebrate cats converted the depressor response to stimulation of the carotid sinus nerve into the definite pressor one described above; as previously, no conspicuous changes in heart rate occurred (Fig. 4). Nembutal anaesthesia. Intraperitoneal injection of nembutal, however, in decerebrate cats did not reverse the depressor response to carotid sinus-nerve stimulation (Fig. 5). In cats, initially anaesthetized with nembutal by intraperitoneal injection, stimulation of the carotid sinu's nerve caused a fall in arterial -blood pressure, Similar results irrespective of frequency or pulse duration of the stimui used. were obtained using an induction coil discharge. Subsequent intravenous
6 264 E. NEIL, C. R. M. REDWOOD AND A. SCHWEITZER injection of g. of chloralose converted the depressor response to carotid sinus-nerve stimulation into a marked rise within approximately 20 min. (Fig. 6). During a period of min. after chloralose injection, responses to stimulation were indeterminate. Chlorat hydrate. In animals anaesthetized by intravenous injection of chloral hydrate, stimulation of the carotid sinus nerve always caused a fall in blood pressure, often accompanied by cardiac slowing. lb~i Fig. 5. Decerebrate cat. Records as in Fig. 4. Tracing A: induction coil stimulation of right carotid sinus nerve (coil distance 15 cm.). Tracing B: repeat stimulation $0 min. after intraperitoneal injection of nembutal (40 mg./kg. body wt.). From these experiments it would appear that: (1) The rise of arterial blood pressure produced by stimulation of the carotid sinus nerve with pulses of short duration ( msec.) or with induction coil discharges in cats under chloralose anaesthesia, is a vasomotor centre response. (2) Pulses of longer duration ( msec.) in chloralosed cats may produce a fall in Arterial pressure. (3) The qualitlative nature of the response to carotid sinus-nerve stimulation is closely related to the choice of anaesthetic. Intheunanaesthetized decerebrate animal, sinus-nerve stimulation causes a fall of arterial blood pressure. The injection of nembutal does not modify this response. Administra-
7 STIMULATION OF THE CAROTID SINUS NERVE 265 tion of chloralose, however, reverses the fall of arterial blood pressure consequent upon sinus-nerve stimulation into a marked pressor response. The carotid sinus nerve is a mixed afferent nerve containing afferents from the baroceptors of the carotid sinus and from the chemoceptors of the carotid body. Comroe & Schmidt (1940) have shown that excitation of the chemoceptors of the carotid body by chemical means is attended by slight pressor effects, tachyeardia and hyperpnoea. Fig. 6. Cat, nembutal. Records from above downwards: respiration, blood pressure, signal, time in 5 sec. Tracing A: rectangular wave stimulation of right carotid sinus nerve (100 cyc./sec., 2 V., 0.1 msec.) before, tracing B: 30 min. after intravenous injection of 01 g. cbloralose. Electrical stimulation of the carotid sinus-nerve trunk might be expected to cause excitation of both types of afferent fibre. There are various possible ways in which chloralose anaesthesia might produce the decisive modification of the response to electrical stimulation: (1) By sensitization of baroceptors which ;eflexly raise the blood pressure. Such baroceptors, functionally inactive under normal conditions, might become prominent in conditions of arterial hypotension. Though the existence of such pressor afferents has been denied (Koch, 1931; Schweitzer, 1937) it was thought necessary to reinvestigate this point. (2) By modifying the response of the vasomotor centre to carotid sinus-nerve stimulation by suppressing the inhibitory effects of baroceptor excitation on the centre. Chemoceptor stimulation would thus be revealed and then produce
8 266 E. NEIL, C. R. M. REDWOOD AND A. SCHWEITZER a rise in arterial blood pressure. (3) By diminishing the excitability of the afferent fibres arising from the baroceptors. (4) By affecting in some way the efferent part of the reflex arc involved in the vasomotor response to carotid sinus-nerve stimulation. Some of these theoretical possibilities have been experimentally investigated. Effect of altering pressure in carotid sinus Absence of pressorfibres in the carotid sinus nerve. This problem was investigated by subjecting one isolated carotid sinus preparation to changes of static internal pressure. Cats under chloralose anaesthesia were used. Both vagi were cut and the carotid sinus nerve of the opposite side was sectioned. Koch (1931) and Schweitzer (1937) showed that a threshold intrasinusal pressure of mm. Hg is required to produce excitation of the baroceptors in the dog. It was therefore decided to maintain an initial pressure of 70 mm. Hg in the isolated carotid sinus in these experiments. Sudden lowering of the intrasinusal pressure from 70 to 0 mm. Hg did not produce any change in systemic blood pressure. It was therefore concluded that the carotid sinus nerve does not contain true pressor fibres arising from baroceptors. The rise of the-arterial blood pressure produced by certain types of electrical stimulation of the sinus n,erve trunk must have been due to some other mechanism. Modification of vasomotor centre response by chloralose. *Nembutalized cats, bilaterally vagotomized, were used in these experiments. The contralateral sinus nerve was cut and the remaining sinus isolated as previously. Raising the intrasinusal pressure from 70 to 220 mm. Hg produced a marked fall in arterial pressure. This response was still obtained over 2 hr. after commencing the experiment (Fig. 7). In the experiment illustrated by Fig. 7, 0.06 g. of chloralose was then injected intravenously. Five minutes later, raising the intrasinusal pressure from 70 to 220 mm. Hg only produced a slight fall in arterial pressure; 20 min. later the response to an increase of pressure in the carotid sinus was completely abolished (Fig. 7). On electrical stimulation of the corresponding carotid sinus nerve, marked pressor responses were obtained. In this type of experiment chloralose did not have access to the baroceptors or to the afferent fibres of the carotid sinus nerve, which mainly receive their blood supply from capillaries of the ascending pharyngeal system. Consequently, the effect of chloralose must have been exerted on structures other than the afferent side ofthe reflex arc. A possible criticism of this conclusion would be that the abolition of the response to a rise of intrasinusal pressure was merely due to death of the baroceptors. However, this experiment was repeated several times with similar results. Complete abolition of the response to static pressure changes in an isolated sinus preparation aftervintravenous injection of chloralose was not invariable, but partial abolition always occurred.
9 STIMULATION OF THE CAROTID SINUS NERVE* 267 Fig. 7. Cat, nembutal. Isolated right sinus preparation. Other buffer nerves cut. Records from above downwards: respiration, blood pressure, hydrostatic pressure in right sinus, signal, time in 5 sec. At A, B and C responses to increase in intrasinusal pressure from 70 to 220 mm. Hg at 0, i and 2 hr. At arrow, intravenous injection of 0-06 g. chloralose. Note greatly diminished response to sudden rise of intrasinusal pressure after 5 min. (D); response completely abolished after 20 min. Fig. 8. Cat, nembutal. Both vagi cut. Isolated left and right carotid sinus preparations. Records as in previous figure. A: responses to left and right intrasinusal pressure rises from 0 to 230 mm. Hg. B and C: responses to intrasinusal pressure rises, 60 min. after intravenous injection of 0 06 g. chloralose. Between C and D inject chloralose into right sinus preparation. D: response to pressure increase in right sinus diminished. E and X: responses to pressure increases in left sinus unaffected.
10 268 E. NEIL, C. R. M. REDWOOD AND A. SCHWEITZER These results presumably explain our failure on many occasions to obtain responses to rises of intrasinusal pressure in chloralosed cats. Invariably, in such animals, stimulation of the carotid sinus nerve trunk produced a pressor response. Thus it would appear that chloralose affects the response of the vasomotor centre or the efferent part of the vasomotor reflex. arc. Obviously, these experiments do not exclude the possibility that chloralose affects the baroceptors in the intact animal. This possibility was next investigated. The effect of chloralose on the response of the baroceptors. Bilateral carotid sinus gravity perfusion preparations were used in these experiments. Cats under nembutal anaesthesia were bilaterally vagotomized. Both carotid sinus preparations were alternately subjected to rises in internal pressure. Typical depressor responses were recorded. Chloralose was then injected intravenously, and it was foutd that the blood-pressure responses to alternate increases of pressure in the perfused sinuses were almost identically diminished (Fig. 8). Chloralose in an amount sufficient to give a final concentration of 003 % was then added to the solution perfusing one carotid sinus. Within 5 min. exposure of that sinus preparation to chloralose the response to an increase in pressure was further reduced, but the response from the other sinus was unchanged. Such an experiment shows that, in addition to a modification of the vasomotor centre response to afferent nerve stimulation seen in cats under chloralose anaesthesia, there is the further possibility of a direct action of the chloralose on the baroceptors themselves. Clearly, the local injection of chloralose into the isolated and perfused carotid sinus can exert no effect on the efferent side of the vasomotor reflex arc İn two chloralosed animals normal depressor responses to rise in intrasinusal pressure were obtained; electrical stimulation of the carotid sinus nerve in these animals caused only a fall in blood pressure. These results were obtained only in animals with perfused carotid-sinus preparations in which there exists a possibility of a gradual decrease of the chloralose concentration in the baroceptor tissue under conditions of continuous perfusion with Ringer-Locke solution. DISCUSSION It is well known that a rise of pressure in the carotid sinus stimulates the baroceptors of the sinus causing a reflex fall in arterial blood pressure. Von Euler, Liljestrand & Zotterman (1941) have shown that such reflex effects may be obtained in the cat when the perfusion pressure is raised in the carotid sinus. It was therefore surprising to find that, in the cat under chloralose anaesthesia, electrical stimulation of the carotid sinus nerve either by means of an induction coil discharge or a rectangular wave electronic stimulating device, can produce dramatic pressor responses.
11 STIMULATION OF THE CAROTID SINUS NERVE 269 In some of these cats, by varying only the pulse duration of the individual stimuli, we were able to elicit either pressor or depressor effects on the arterial blood pressure. This differentiation of the effects of carotid sinus-nerve stimulation may be related to the different excitability time constants of the fibres composing the nerve trunk. Zotterman (1935) has presented evidence of the presence of small and large myelinated fibres in the carotid sinus nerve of cats, assuming that the larger fibres are derived from the baroceptors and the smaller components from the chemoceptors. A detailed histological examination of the composition of the carotid sinus nerve in various species is at present in progress. Analysis of the pressor response obtained in cats under chloralose anaesthesia has shown it to be an effect involving activity of the vasomotor centre. The experiments on the isolated carotid sinus preparations prove conclusively that the pressor response to sinus nerve stimulation was not due to stimulation of true pressor fibres from the baroceptors. The explanation of the pressor effect of electrical stimulation of the carotid sinus nerve in chloralosed cats, therefore, involved a consideration of a possible abolition, partial or complete, of the classical inhibitory influence of the carotid sinus mechanism on vasomotor centre activity, and/or a sensitization of chemoceptor effects on the vasomotor centre. It is shown in our experiments on the effects of perfusion of solutions containing chloralose through the isolated carotid sinus that the site of action of the anaesthetic could not have been the peripheral efferent side of the reflex arc involved in these vasomotor phenomena. Evidence was presented indicating that chloralose inhibits the effects of baroceptor stimulation on the vasomotor centre. In animals with both carotid sinuses isolated from the circulation, responses to alternative intrasinusal pressure rises were invariably diminished following intravenous injection of chloralose, as compared with the results, previously obtained in the same animal under initial nembutal anaesthesia. It was further shown, by perfusion of Ringer-Locke containing chloralose through one isolated carotid sinus, that the response of that sinus preparation to an augmentation of perfusion pressure was markedly diminished, thus showing that chloralose also decreased the sensitivity of the baroceptors to pressure stimulation. It is therefore concluded that intravenous injection of chloralose in intact cats both diminishes the sensitivity of the baroceptors to hydrostatic pressure changes and inhibits the vasomotor centre response to baroceptor stimulation. Under such conditions, carotid sinus-nerve trunk stimulation essentially excites only the afferents arising from the chemoceptors of the carotid body, causing a rise of blood pressure. On several occasions, section of the carotid sinus-nerves in cats under
12 270 E. NEIL, C. R. M. REDWOOD AND A. SCHWEITZER chloralose anaesthesia, both vagi being already cut, has caused a fall of arterial blood pressure. Such results indicate the preponderance of tonic chemoceptor afferent discharge upon the vasomotor centre. If this interpretation of our experimental results be correct, it is incumbent upon us to explain the fact that occlusion of both common carotid arteries in cats under chloralose anaesthesia always causes a marked rise in arterial pressure. Much of this effect is, in our belief, due to -the stimulation of the chemoceptors of the carotid body by the changes in the composition of the stagnant blood contained therein. Marked depressor responses to rises in intrasinusal pressure can occasionally be obtained in cats under chloralose anaesthesia, but such effects were only. recorded when electrical stimulation of the carotid sinus nerve trunk produced a fall in blood pressure, especially when stimuli of long duration were used. Von Euler, Liljestrand & Zotterman (1941) have also obtained depressor responses to rises inintrasinusal pressure, using cats under clhloralose anaesthesia. Recent work has shown that the results of these experiments on cats cannot be obtained in the case of the dog or the rabbit. SUMMARY 1. Stimulation of the carotid sinus nerve trunk in cats under chloralose anaesthesia by means of induction coil discharges or a rectangular wave electronic stimulator produced marked rises in arterial blood pressure with pulses of short duration ( msec.), and hyperpnoea, but only insignificant changes in heart rate. Pulses of longer duration ( msec.) occasionally caused a fall in blood pressure. These effects involved the activity of the vasomotor centre. * 2. Stimulation of the carotid sinus nerve in unanaesthetized decerebrate or in nembutalized cats, or in cats under chloral hydrate anaesthesia, invariably lowered the blood pressure, irrespective of the duration of the stimuli used. Subsequent intravenous injection of chloralose in such animals converted the previous depressor response to stimulation into a pre'ssor response. 3. The carotid sinus nerve does not contain pressor fibres. 4. Responses to rises of intrasinusal pressure in nembutalized cats were diminished by intravenous injection of chloralose. In addition, perfusion of the isolated carotid sinus with Ringer-Locke solution containing chloralose diminished the response to increase in hydrostatic pressure. 5. Chloralose diminishes in cats the sensitivity of the vasomotor centre and of the baroceptors of the carotid sinis to changes of intrasinusal pressure. 6. The pressor response to electrical stimulation of the carotid sinus nerve trunk in cats under chloralose anaesthesia is due to excitation of the chemoceptor afferents contained in the nerve.
13 STIMULATION OF THE CAROTID SINUS NERVE 271 REFERENCES Bronk, D. W. & Stella, G. (1932). J. cell. comp. Physiol. 1, 113. Comroe, J. H. & Schmidt, C. F. (1940). Physiol. Rev. 20, 115. Hering, H. E. (1927). Die Karotissinusreflexe auf Herz und Gefasse. Leipzig: Steinkopff. Heymans, C., Bouckaert, J. J. & Regniers, P. (1933). Le Sinus Carotidien et la Zone Homol4gue Cardio-Aortique. Paris: Doin et Cie. Koch, E. (1931). Die reflektorische Selbststeuerun.g des Kreislaufes. Leipzig: Steinkopff. Moissejeff, E. (1926). Z. ges. exp. Med. 53, 696. Neil, E., Redwood, C. R. M. & Schweitzer, A. (1948). J. Physiol. 107, 8P. Schweitzer, A. (1937). Die Irradiation Autonomer Reflexe. Basle: Karger. Von Euler, U. S., Liljestrand G. & Zotterman, Y. (1939). Skand. Arch. Physiol. 83, 132. Von Euler, U. S., Liljestrand, G. & Zotterman, Y. (1941). Acta Physiol. Scand. 2, 1. Zotterman, Y. (1935). Skand. Arch. Physiol. 72, 73.
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